Wednesday, May 23, 2012

Individuals vary in their phenotypic traits. The importance of this truism has long been recognized in the field of evolutionary biology; without such heritable variation, there would be no evolution, as Darwin rightly pointed out. In contrast, the study of ecology seems to have often blipped along merrily, while quietly sweeping variation within species under the rug. Perhaps it wasn’t naively that ecologists regarded all individuals within a species as identical when constructing models of species competition, predation, etc. but simply from a need to reduce complexity. When I began my MSc degree, back in 2006, the potential importance of individual variation for ecological dynamics was finally receiving some long-deserved attention.

At that point in time, we had a collection of rigorous studies showing effects of genetic diversity on population, community and even ecosystem variables – everything from primary productivity, to nutrient cycling, to community resilience and species composition might be affected. However, this result was by no means universal – and studies that did find positive genetic diversity effects also varied in the magnitude of the effects identified. Clearly, we knew that genetic diversity could be important to ecology, but we had little predictive understanding of these effects.

What mechanisms generate diversity effects? How does environmental context matter? Why does genetic diversity produce effects in some studies but not others? These are the kinds of questions that my MSc supervisor, Dr. Mark Vellend, and I pondered. We were particularly intrigued by the circumstantial evidence from studies of marine eelgrass (i.e. Reusch et al. 2005. PNAS 102:2836-2831, Hughes & Stachowicz 2004. PNAS 101:8998-9002) that genetic diversity effects might only be revealed under poor conditions (e.g. stress or disturbance). Mark and I wondered if this might be a general result – did diversity matter more under unfavorable conditions, which might magnify genetic differences among individuals?

We designed an experiment using locally collected (on the British Columbia coast), asexual dandelions to investigate this possibility. In the spring of 2007, we created replicate dandelion populations of low (1-genotype), medium (2 genotypes) or high (4-5 genotypes) genotypic richness under field conditions. This diversity treatment was fully crossed with an environmental treatment: dandelions grew in either unfavorable “mowed lawns”, or in recently tilled, favorable “fallow fields”. As you can see from the pictures, these habitat types were completely randomized across the plots (we created the fallow plots as needed, by turning over the sod) and the initial growth environment varied hugely depending on habitat. In contrast to the fallow field, plants in the mowed lawn were surrounded by other species and regularly disturbed by clipping.

Planting the dandelions in a grid pattern in each plot, we were able to assess seed number and total leaf area (a measure of plant size/biomass) for each individual over the course of two years. We found that genotypic diversity enhanced population performance universally, but to a greater degree in the fallow field. For example, the gain in plot performance with diversity, from low- to high-richness plots, was 52% vs. 20% for leaf area and 31% vs. 23% for seed number. Large genotypes dominated in the fallow field leading to positive selection effects and significant overyielding. In the mowed lawn, where performance was limited, there was evidence for complementarity among genotypes, but no overyielding. Hence, our diversity effects, while clearly environment-dependent, were stronger in the more favorable environment - contrary to our prediction. While we don’t have a precise explanation for this result, our conjecture is that the larger size of and the stronger competition among genotypes in our fallow field enhanced genotypic differences. There is some evidence for this in the data.

Unfortunately the capacity of dandelions to form multiple rosettes, all attached to the same taproot, eventually led to difficulties identifying “individuals”. After about 2 years, despite our handy grid system, the plants had become so large that figuring out who was who in our experimental plots became next to impossible. While this meant that we could no longer determine the underlying mechanisms, which requires data on individuals, we could still examine the plot-level diversity effects. When we terminated the experiment in the summer of 2010, genotypic diversity effects were still strong and present. In fact, these effects increased in strength with time – just as has been found for species diversity effects on productivity!

A complementary field seed germination trial we carried out in 2008 revealed that differences in performance (i.e. seed production) among genotypes in different treatments should carry over into the next generation. Hence, genotypic diversity effects may be more than merely transient dynamics, and could have long-term ecological consequences in our system. As I’ve also discussed, these effects were sensitive to environmental-context, possibly relating to the frequency of disturbance and strength of intraspecific competition. While it remains possible (and likely) that genetic diversity may have strong population-level consequences only under stress or disturbance in some systems, our study suggests another set of circumstances that might reveal important diversity effects: dense, monospecific stands of a focal species, with intense competition among individuals.

Friday, May 11, 2012

I have a question for the readers of this blog - something I need to "poll" you on.
First, a little bit of background. When I was a beginning graduate student at the University of California at Davis, a faculty member on my committee asked me whether I intended to be "a consumer, or a producer, of theory". His goal was to determine what kind of statistics or pure math classes he should direct me to take, which is a decision every student is faced with. My goal at the time was to do empirical tests of theory (a vague concept - see below), so I casually said "consumer" and went for the statistics options. Fourteen years later, I look back at that decision as both correct, and unfortunate. Correct, in that the solid grounding in statistics that I gained has served me well in the following years. Unfortunate, in that it perpetuates an either/or view of empirical and theoretical work that has come back to haunt me this spring.
Here's why: Eva Kisdi and U. Helsinki has invited me to give a series of lectures (6 hours) in August on the intersection of theory and empirical work on speciation. Naively agreeing, I now need to figure out how theory and empirical approaches actually intersect. Turns out to be harder than I expected for several reasons. I raise two questions here, and invite readers to respond:

1) What does it mean for theory and data to intersect? I see several options, but would welcome additional ideas here:
A) Theory can make predictions about what is possible, empiricists can test whether the predicted phenomenon actually exists. This is a weak test because it does not actually show that the theoretical justification is correct, only that the end product is correct. Many different models might generate the same pattern (c.f., ecological neutral theory's "predictions"). Another problem is that many models predict many possible outcomes, depending on exact parameter values. For instance in my graduate work I "tested" the theoretical prediction that intraspecific competition drives disruptive selection (Bolnick 2004 Evolution), but really the model predicts either disruptive OR stabilizing selection, depending on parameter values that I didn't (couldn't) measure. I can think of a number of examples in the speciation literature, but would welcome suggestions as to your favorites.
B) Theory can make quantitative predictions that can be exactly tested for quantitative fit (see Optimal Foraging Theory work in the 70's for example) - I can't think of examples in the speciation literature: suggestions welcome.
C) Empirical data can demonstrate that something occurs biologically (e.g., sympatric speciation), and the models can be developed to formalize our thoughts about how this works. Examples include Schliewen's Nature paper on Cameroon cichlids that made sympatric speciation respectable again (for some people) and the subsequent irrational exuberance about the topic among theoreticians.
D) Empirical data can be used to parameterize a model to make biologically informed predictions (see my new paper with Mark Kirkpatrick in Current Zoology.
E) a model can be built for strictly statistical purposes to estimate parameters using empirical data. For instance, coalescent theory has been used to build analysis programs (e.g., Migrate, IM) that are used to estimate parameters (timing of divergence, subsequent gene flow) relevant to speciation. Lots of examples, mostly in the area of molecular evolution and phylogenetics and population genetics, all of which sometimes spill over into the speciation literature.
F) The holy grail: All of the above. Make an empirical observation, build a model to explain it. Parameterize the model with independent data to make a specific novel prediction, test this empirically. Are there ANY examples?

2) What are BEST examples you can think of, of papers that actually fuse theory and empirical data to address questions in speciation?

Sunday, May 6, 2012

I first started working in Trinidad in 2001 and, in 2002, I
started sampling guppies from large numbers of sites from two rivers (Marianne
and Paria) on the north slope of the northern mountain range. These samples
were used to characterize variation in traits and genetic makers so as to infer
how interactions between selection and gene flow influenced adaptation. This first
project ended in 2004 and it had been great fun exploring, climbing over
waterfalls, and trying to find viable guppy populations throughout the
spider-web network of these two nearly pristine rivers. I therefore figured it
would be a good idea to come up with an excuse to keep visiting. My students
have since done many projects but I also created a project of my own to make
sure that I came back every year and went to the coolest remote sites. I
therefore selected 10 sites to start a long-term sampling protocol– ten sites
that were not only biologically interesting but that required walking long
distances in beautiful streams and camping in remote areas. This year marked
the 11th year visiting these sites and I have now amassed 5327
guppies (about 50 per year) from these 10 sites alone (many more have been
sampled from other sites). The idea is to use these long-term samples to study eco-evolutionary
processes as they act through time and space. With more than 10 years of
working in Trinidad, it seems a good time to go back to my notes and dig up a
few interesting events that occurred.

﻿

I think I see a guppy.

2012: This afternoon, Gregor (Rolshausen) went off to catch
fish. When he came back to our house (Indra’s) after dark, he had a 2 m long
snake with him. Apparently it had been tangled up in his windshield wipers when
he had gotten back to his car. He wasn’t sure if it was alive or dead – or what
kind it was – and so he had gone and asked the guards (he had parked his car at
a water authority – WASA – station) if they could shine a light on it for him. The
guards were very excited and apprehensive and brought a heavy metal pipe with
them to use as a weapon. When they saw the saw the snake, however, their
braveness evaporated and none would go anywhere near it. When Gregor removed it
from the wipers they said, accusingly, “what are you, some kind of snake man or
something”?

Snake man.

2011: Stayed home (Indra’s) and processed fish. The crew
(Felipe Perez, Kiyoko Gotanda, and Maryse Boisjoly) drove off the Simla to
check their email. I was in the kitchen when they returned. “Andrew, come quick
right now” they shout at me. They seem all crazy, almost panicked.”Damn,” I
think “Who’s hurt.” But then it becomes clear they are excited rather than
scared. “You’ve gotta come here right now you’ve gotta see this.” “Do I need my
camera,” I ask. “Definitely!” Ah, so it is something cool. I approach the car
but rather than all of them piling back in to driver somewhere, they sort of
stand away, as though the cool thing is actually in the car. Sure enough, there
on the shelf below the back window is a tropic screech owl. It seems that they
were driving along the road and the owl actually flew in the window, hit
Felipe’s head, and then the back window. They had all yelled in surprise and
pulled the car over to figure out what happened. The owl had seemed rather
dazed – sort of sitting there but drooping, with its eyes closed – and so they
simply drove back to Indra’s. We spent the next half hour taking pictures (just
a few) and watching as the owl slowly seemed to recover. It eventually flew off
- quite a unique experience.

The owl in the car.

2008: I walked up the Petit Marianne twice this year. Each
time while walking through the village of Avocat, a healthy looking, smallish,
golden dog started walking with us. He didn’t seem needy, or begging, or
aggressive – it just seemed like he wanted to go for a walk. Dogs rarely follow
us in this manner in Trinidad, and those that do invariably give up soon - but
not this dog. He was right with us all the way to the falls, then up over the
hill, and then all along the length of the river with us for several hours. At
first I wasn’t favorably inclined to having a dog along, but it was such a consistent
and pleasant companion, that I warmed to it. When we stopped for lunch, I gave
it a PBJ sandwich – but it wasn’t interested. This piqued my interest even more
– the dog clearly wasn’t along just for the food. After sampling, the dog
accompanied us back to our other sampling sites on the main stem of the Marianne.
He would curl up and sleep beside our equipment while we were sampling. Then it
stayed with us again on the way out until we reached Avocat, where it
disappeared. Our second day on the Petit Marianne, he did the whole hike with
us again and then stayed by the car as we took our gear off. Amazing, he would
stand in the way of cars coming down the road and growl at them – as though he was
protecting us. Needless to say, we were beginning to think this dog wanted to
adopt us; so when we drove off, we did so quickly. It immediately ran after us
at top speed, really fast actually, barking plaintively. In other
circumstances, I might have kept it. A final note: when the dog was facing off
with cars on the road, another man was there waiting for a ride. He lived at
Avocat and knew the dog. I related to him how the dog had reacted to us on both
of our hikes and his simple answer was: “Oh that dog – he likes white folks.”

Our campsite on the Paria River.

2006: Yesterday I took my annual camping trip into the Paria,
this time with Martin Turcotte, Ian Paterson, and Paul Bentzen. We saw lots of
cool stuff, particularly two fer-de-lances, both of which I walked within
inches of before someone behind me spotted them. I must look very carefully
only where I put my feet. This stops me from stepping on snakes but I miss many
that are VERY close. In fact, this is at least the fourth snake I have walked
right past (yes, I have seen others before walking past them). We saw one on
the way into the camping site and one on the way out (see photo). This second
time, it was becoming dark and watching for snakes given our new-found piety
made us go quite a bit slower. [As of 2006, I have now seen 8 fer-de-lances in
approximately 12 weeks of work in Trinidad.] Oh, and lest I forget: a major
breakthrough on the splinter! I was squeezing hard all day getting puss out.
Eventually I squeezed so hard that the pus was welling up like magma and all of
a sudden, pop, out comes the splinter – floating on the pus like the negative
of a marshmallow floating on hot chocolate.

Just missed.

2005: We found two small pools (1-2 m squared) right at the
silk cotton tree, each with vast numbers of guppies. We captured 41 females, 32
males, and hundreds of juveniles in one and 42 females and 31 males in the
other. These were probably less than half of the actual number of guppies in
each pool. These pools are isolated from the mainstem although they would be
flooded in moderately high water. The males were very colourful in relation to
mainstem guppies just a few yards away. They are probably the most colourful
guppies I have seen, although the amount of orange is low. Instead they have
large patches of yellow, pink, purple, etc. I suspect that conditions in these
pools are very different from the main stem of the river and that the evolution
of high colour owing to female choice proceeds within them during periods of
isolation only to be reversed owing to predation when they are washed out
during the next flood. It would be very interesting to examine the dynamics of
this interaction. I took a sample with this in mind. (Note: I still haven’t done
this examination as of 2012).

Paul Bentzen catching guppies.

2003:
... At this point David Reznick had worked his way down the cliff and reached
the tree. With remarkably little hesitation he sacrificed his testicles to the
6 inch tree by leaping forward, straddling it, and sliding ungracefully
downward, taking the bark with him as he went. Mike Kinnison, who was just
above, heard and saw David’s farewell to future children and filed this away
for future reference – which turned out to be needed in the immediate future. I
climbed up the steep rocks to the base of the sacrificial tree, with Mike
immediately above. He lowered the pack and then his eyes lifted to survey the
tree, as though seeing it for the first time. “I’m supposed to jump to that?”
he asked, knowing the answer but somehow not accepting. All he could now see in
his mind’s eye was David spread-eagled on the tree loudly decrying the state of
his testicles. “Is there any other way?” “Well” I said “I suppose you could go
up and around but I don’t know if you will find a way that is any easier.” Mike
looked uncertain. He knew he didn’t want to go back up that horrible cliff but
he also knew he wanted to have children. His eyes moved up and down the tree as
I waited not-so-patiently below, as if I might catch him should his jump not go
so well. After some moments of hesitation and in a wondrous display of
counter-intuition, he leaned out and fell slowly forward until his hands were
on the tree and his feet, almost horizontal behind him, were on the ledge.
Perched there, with no way back, his eyes clinically scanned the cliff below
him. “Maybe I could just walk down the cliff” he asked in defiance of all
logic. “Damn it Mike, jump” And jump he did, ever so much more graciously than
had David, informed no doubt by David’s demonstration of how not to do it.
(Note: Both David and Mike have subsequently had children.)

The site of David's and Mikes' sacrifice.

Stoies abound – and these are
just a few of them. Here’s looking forward to having new ones in the years to
come.